Abstract

INTRODUCTION

The Amazon region is undergoing an intense process of occupation, with significant changes in patterns of land use through the clearing and burning of large scale forested areas.⁹9. Fearniside PM. Desmatamento na Amazônia: dinâmica, impactos e controle. Acta Amaz. 2006;36(3):365-400. DOI: http://dx.doi.org/10.1590/S0044-59672006000300018
http://dx.doi.org/10.1590/S0044-59672006... These burnings are responsible for significant emissions of aerosol particles into the atmosphere, having both direct and indirect effects on the climate and the functioning of the Amazonian ecosystem.³3. Artaxo P, Oliveira PH, Lara LL, Pauliquevis TM, Rizzo LV, Pires Jr C, et al. Efeitos climáticos de partículas de aerossóis biogênicos e emitidos em queimadas na Amazônia. Rev Bras Meteorol. 2006;21(3):1-22. The population’s health is significantly affected, especially in the region of the deforestation arc.⁷7. Carmo CN, Hacon SS, Longo KM, Freitas S, Ignotti E, Artaxo P, et al. Associação entre material particulado de queimadas e doenças respiratórias na região sul da Amazônia brasileira. Rev Panam Salud Publica. 2010;27(1):10-6. DOI: http://dx.doi.org/10.1590/S1020-49892010000100002
http://dx.doi.org/10.1590/S1020-49892010... , ⁸8. Castro H, Gonçalves KS, Hacon SS. Tendência da mortalidade por doenças respiratórias em idosos e as queimadas no Estado de Rondônia/Brasil – período entre 1998 e 2005. Cienc Saude Coletiva. 2009;14(6):2083-90. DOI: http://dx.doi.org/10.1590/S1413-81232009000600015
http://dx.doi.org/10.1590/S1413-81232009...

Atmospheric conditions considered to be clean during the Amazonian rainy season are altered during the dry season due to the emissions of aerosol particles from burning pasture and forests. This has significant implications at a local, regional and global level.²2. Artaxo P, Gatti LV, Leal AMC, Longo KM, Lara LL, Procópio AS, et al. Química atmosférica na Amazônia: A floresta e as emissões de queimadas controlando a composição da atmosfera amazônica. Acta Amaz. 2005;35(2):185-98. DOI: http://dx.doi.org/10.1590/S0044-59672005000200008
http://dx.doi.org/10.1590/S0044-59672005... During the rainy season, when natural biogenic emissions predominate, the concentration of particle mass is < 10 microns (PM₁₀) and around 10 µg/m³, with a concentration of 300 particles cm⁻³. Coarse fraction particles (with diameters between 2.5 and 10 microns) represent 80% of the total particle load in the atmosphere. In regions severely affected by biomass burning, the particle mass concentration rises to 300 to 600 µg m⁻³, as the number of particles climbs to 15,000 to 30,000 particles cm⁻³, and the fine particles (< 2.5 microns, so-called PM_2.5) becomes predominant over the coarse particles.²2. Artaxo P, Gatti LV, Leal AMC, Longo KM, Lara LL, Procópio AS, et al. Química atmosférica na Amazônia: A floresta e as emissões de queimadas controlando a composição da atmosfera amazônica. Acta Amaz. 2005;35(2):185-98. DOI: http://dx.doi.org/10.1590/S0044-59672005000200008
http://dx.doi.org/10.1590/S0044-59672005...

In contrast to urban environments, in which atmospheric pollution is characterized by chronic exposure, biomass burning in the Amazon is characterized by exposing the health of the population to elevated levels for an average period of three to five months per year, linked to low levels of rainfall.⁷7. Carmo CN, Hacon SS, Longo KM, Freitas S, Ignotti E, Artaxo P, et al. Associação entre material particulado de queimadas e doenças respiratórias na região sul da Amazônia brasileira. Rev Panam Salud Publica. 2010;27(1):10-6. DOI: http://dx.doi.org/10.1590/S1020-49892010000100002
http://dx.doi.org/10.1590/S1020-49892010... The regions most affected by emissions from biomass burning are concentrated along the so-called deforestation arc (Acre and Rondônia, Southern Amazonas, Northern Mato Grosso and Eastern Pará), following the courses of the highways. These emissions affect the health of the population of the almost the entire Amazon basin, as the smoke from the burning consists primarily of fine particles which are easily transported over long distances.³3. Artaxo P, Oliveira PH, Lara LL, Pauliquevis TM, Rizzo LV, Pires Jr C, et al. Efeitos climáticos de partículas de aerossóis biogênicos e emitidos em queimadas na Amazônia. Rev Bras Meteorol. 2006;21(3):1-22.

Inhalable particles are < 10 µm and can reach various levels of the human respiratory system. Particles between 2.5 and 10 µm mainly come to rest in the upper part of the respiratory system and the main bronchi. Fine particles (< 2.5 µm) may reach further into the respiratory system, as far as the pulmonary alveoli.¹⁰10. Gomes MJM. Ambiente e pulmão. J Pneumol. 2002;28(5):261-9. DOI: http://dx.doi.org/10.1590/S0102-35862002000500004
http://dx.doi.org/10.1590/S0102-35862002... Epidemiological studies show consistent increases in hospital admissions and deaths from respiratory and cardiovascular disease, related to exposure to pollutants present in the atmosphere in different areas of the planet. This mainly occurs in the most susceptible groups (children the elderly and those with a history of cardiorespiratory disease), even at levels of exposure deemed safe by environmental legislation.⁵5. Bell ML, Peng RD, Dominici F. The exposure–response curve for ozone and risk of mortality and the adequacy of current ozone regulations. Environ Health Perspect. 2006;114(4):532-6. DOI: http://dx.doi.org/10.1289/ehp.8816
http://dx.doi.org/10.1289/ehp.8816... , ¹⁸18. Rosa AM, Ignotti E, Hacon SS, Castro HA. Análise das internações por doenças respiratórias em Tangará da Serra – Amazônia brasileira. J Bras Pneumol. 2008;34(8):575-82. DOI: http://dx.doi.org/10.1590/S1806-37132008000800006
http://dx.doi.org/10.1590/S1806-37132008...

Worldwide mortality from respiratory disease reached almost 13 million children under 5,95% of which were in developing countries. Respiratory disease is responsible for around 10% of deaths in children less than a year old and for more than 50% of hospital admissions of under 5s in Brazil.¹⁵15. Organización Panamericana de La Salud. Evaluación de los efectos de la contaminación del aire en la salud de América Latina y el Caribe. Washington (DC); 2005. Exposure to atmospheric pollution is related to systemic effects such as activation of inflammatory pathways and oxidative stress,¹⁶16. Pope III, CA. Air Pollution and Health: Good News and Bad. N Engl J Med. 2004;351(11):1132-4. DOI: http://dx.doi.org/10.1056/NEJMe048182
http://dx.doi.org/10.1056/NEJMe048182... arterial vasoconstriction and immunological changes,¹⁴14. Nell AE, Diaz-Sanchez D, Hiura T, Saxon A. Enhancement of allergic inflammation by the interaction between diesel exhaust particles and the immune system. J Allergy Clin Immunol. 1998;102(4Pt1):539-54. DOI: http://dx.doi.org/10.1016/S0091-6749(98)70269-6
http://dx.doi.org/10.1016/S0091-6749(98)... and blood coagulation factors.⁶6. Brook RD, Brook JR, Urch B, Vincent R, Rajagopalan S, Silverman F. Inhalation of fine particulate air pollution and ozone causes acute arterial vasoconstriction in healthy adults. Circulation. 2002;105(13):1534-6. DOI: http://dx.doi.org/10.1161/01.CIR.0000013838.94747.64
http://dx.doi.org/10.1161/01.CIR.0000013... There are few Brazilian studies which assess the effects of exposure to aerosols from burning biomass on cardiorespiratory function and mortality in children and elderly in the Brazilian Amazon.⁸8. Castro H, Gonçalves KS, Hacon SS. Tendência da mortalidade por doenças respiratórias em idosos e as queimadas no Estado de Rondônia/Brasil – período entre 1998 e 2005. Cienc Saude Coletiva. 2009;14(6):2083-90. DOI: http://dx.doi.org/10.1590/S1413-81232009000600015
http://dx.doi.org/10.1590/S1413-81232009... , ¹²12. Ignotti E, Valente JG, Longo KM, Freitas SR, Hacon SS, Artaxo Netto P. Impact on human health of particulate matter emitted from burnings in the Brazilian Amazon region. Rev Saude Publica. 2010;44(1):121-30. DOI: http://dx.doi.org/10.1590/S0034-89102010000100013
http://dx.doi.org/10.1590/S0034-89102010... Research applying to the Amazon region has only recently been carried out.

The aim of this study was to analyze the relationship between exposure to fine particles emitted by burning biomass and hospital admissions for respiratory disease in children.

METHODS

This was a descriptive study with ecologic time series design of hospital admissions for respiratory disease (Chapter X of ICD-10, codes J00 to J99) in children aged nine and under, resident in Manaus, between 2002 and 2009. Those aged under 29 days old were excluded from the data as the rates of admission were related to birth and not necessarily to exposure to atmospheric pollution. This age group was selected as it represents those individuals most vulnerable to diseases of the respiratory apparatus and the effects of atmospheric pollution. Manaus was chosen as it is a large urban center in the central Amazon, characterized by intense urban expansion and population growth over the last three decades. Hospitalizations reflect exposure to urban pollution originating from industry and vehicles, in addition to biomass burning.

The climate in Manaus is predominantly tropical and rainy. The rainy period occurs between January and April, with March having the highest levels of precipitation (a mean of 310 mm). The dry period is between July and September, with august being the driest month (mean of 50 mm). May and June and October and December are considered to be periods of transition. It rains an average of 190 days per year, resulting in a total accumulated average of 2,280 mm of rain. The relative humidity of the air is high and during the rainy season has a mean of around 88%, and 77% in the dry season. Mean monthly temperatures are stable, varying between 26°C and 28°C. Manaus occupies an area of 11,401 km²2. Artaxo P, Gatti LV, Leal AMC, Longo KM, Lara LL, Procópio AS, et al. Química atmosférica na Amazônia: A floresta e as emissões de queimadas controlando a composição da atmosfera amazônica. Acta Amaz. 2005;35(2):185-98. DOI: http://dx.doi.org/10.1590/S0044-59672005000200008
http://dx.doi.org/10.1590/S0044-59672005... , approximately 592.19 km²2. Artaxo P, Gatti LV, Leal AMC, Longo KM, Lara LL, Procópio AS, et al. Química atmosférica na Amazônia: A floresta e as emissões de queimadas controlando a composição da atmosfera amazônica. Acta Amaz. 2005;35(2):185-98. DOI: http://dx.doi.org/10.1590/S0044-59672005000200008
http://dx.doi.org/10.1590/S0044-59672005... of urban area. According to the 2010 population census, the city of Manaus has 1,802,525 inhabitants, of which 99.5% live in the urban area. Children under nine represent around 18% of the population. Manaus has 54% of the entire state population, which is 3,350,773 inhabitants. It has a municipal human development index (HDI-M) of 0.774, a little above the national average (0.766). The city has 17 general hospitals, seven of which are public, and ten private, according to data from the National Register of Health Facilities (CNES). As of December 2009, the percentage of the population covered by primary health care models was 45.4% (Family Health Program – PSF; Community Agents Program – PACS). ^aaMinistério da Saúde. DATASUS. Cadastro Nacional de Estabelecimentos de Saúde. Brasília (DF); 2010 [cited 2010 Dec 15]. Available from: http://cnes.datasus.gov.br/

The data collected on hospital admissions were secondary, obtained from the Datasus database. ^bbMinistério da Saúde. DATASUS. Sistema de Informações Hospitalares. Brasília (DF); 2010 [cited 2010 Dec 16]. Available from: http://www2.datasus.gov.br/SIHD/ Analysis was limited to hospital admissions due to the lack of reliable systemized data on other levels of care, such as outpatient or emergency care, in the city and state health care network in Manaus, as noted in a survey preceding the fieldwork. Information related to primary health care indicators were obtained from the Primary health Care Information System (SIAB). ^ccMinistério da Saúde. DATASUS. Sistema de Informação de Atenção Básica. Brasília (DF); 2010 [cited 2010 Dec 16]. Available from: http://siab.datasus.gov.br/SIAB/index.php

Levels of PM_2.5 were estimated by measuring aerosol optical density using the MODerate Resolution Imaging Spectroradiometer (MODIS) onboard NASA’s Terra and Aqua satellites. Estimates of PM_2.5 were produced based on aerosol optical density (AOD), according to the method developed by Paixão ^ddPaixão MMA. Propriedades ópticas de aerossóis naturais e de queimadas da Amazônia [dissertação de mestrado]. São Paulo: Instituto de Física da USP; 2011. (2011), for aerosols from burning biomass in the Amazon. The city of Manaus did not have enough surface stations to monitor concentrations of particulate material. Information on population age was provided by the Instituto Brasileiro de Geografia e Estatística (IBGE – Brazilian Institute of Geography and Statistics). Data on relative humidity, mean temperature and precipitation were obtained from the Instituto Nacional de Meteorologia (National Meteorological Institute). Estimates on the number of fires and the area deforested were obtained from a publicly available database on the website of the Instituto Nacional de Pesquisas Espaciais (INPE – National Institute of Space Research). ^eeMinistério da Ciência e Tecnologia; Ministério do Meio Ambiente. Instituto Nacional de Pesquisas Espaciais. SIG Queimadas: monitoramento de focos. Brasília (DF); 2010 [cited 2010 Nov 01]. Available from: http://www.dpi.inpe.br/proarco/bdqueimadas/

The data were collected daily. The Modis censors were not able to accurately estimate AOD on very cloudy days, which contributed to the absence of measurements on these days. This pattern of cloud is common in the Amazon, especially during the first eight to ten weeks of the year. To avoid this lack of information in the time series, it was decided to organize the database by weeks and months.

Hospital morbidity was considered a dependent variable and grouped in the sum of hospitalizations per week (simple count of how many children were admitted each week) and mean monthly rates of hospital admission for respiratory disease (rate of hospitalization in unders per 1,000 inhabitants). The independent variables were: mean weekly and monthly estimates of PM_2.5; weekly and monthly meteorological data of mean air temperature, mean relative humidity and total precipitation; and the weekly and monthly sum of estimated fires. Descriptive statistics were calculated to describe the behavior of the variables during the period in question. In order to verify the relationship between fine particulate material, the meteorological variable and the outcome variable, Pearson linear correlation coefficients (r) were calculated, with a 95% confidence interval. Multiple linear regression models were applied ( Y = a + b₁x₁ + b₂x₂ +... + b_nx_n ). As a measure of quality of fit, the coefficient of determination (R²2. Artaxo P, Gatti LV, Leal AMC, Longo KM, Lara LL, Procópio AS, et al. Química atmosférica na Amazônia: A floresta e as emissões de queimadas controlando a composição da atmosfera amazônica. Acta Amaz. 2005;35(2):185-98. DOI: http://dx.doi.org/10.1590/S0044-59672005000200008
http://dx.doi.org/10.1590/S0044-59672005... ) was used and values above 5% were considered significant. Residue analysis was applied as a measure of the model’s quality of fit. The statistical analysis was carried out using SPSS version 17.0 software.

RESULTS

There were 61,707 hospital admission registered for respiratory disease in children aged under nine years and over 26 days. Hospitalizations for respiratory disease was the most prevalent cause of hospital admission: in children < one year old, 46.6%; aged between one and four, 39.6%; aged five to nine, 20.6%. Male children represented 61% of hospitalizations registered during the period of the study. On average, hospitalization for respiratory disease, in children, represented 67% of hospital admissions for this cause when viewed by age group. Pneumonia (J12, J15 and J18) was the principal cause for children being admitted (45.2%), followed by influenza (J10, 18.2%) and asthma (J45, 17.9%) (Table 1).

The highest monthly rates for hospitalization for respiratory disease in children were observed in the rainy season, and April was the month with the highest mean throughout the period, with hospital admission rates of 2.51/1,000 children. Monthly hospitalization rates varied between 0.48/1,000 children (January/2009) and 3.53/1,000 children (April 2003).

There were 836 fires detected, captured by the Noaa, Aqua and Terra and Goes satellites, and Meteosat, available in the INPE website. Among the 62 municipalities in the Amazon, Manaus was 26^th in terms of the number of fires (0.7% of the total). There were 129,240 fires detected between 1^st January 2002 and 31 December 2009 in the State of Amazonas. The municipalities with the highest rates of incidence (Lábrea, Apuí and Manicoré) are located in the south of the state (Figura 1). The dry period, between August and October, coincided with the greatest incidence of fires (70% of all fires detected in the municipality).

The highest PM_2.5 concentrations for the Manaus region (mean of 20.6 µg/m³) were observed between August and November, the dry season and that with the most burning. Mean PM_2.5 was 13 µg/m³ in the rainy season. Estimates of mean monthly PM_2.5 concentrations vary between 8.7 µg/m³ (April/2002) and 29.2 µg/m³ (November/2002). Annual PM_2.5 levels stayed relatively constant (mean 15 µg/m³).

Upon analyzing the Pearson correlations, there was a positive, significant association between hospitalizations and relative humidity, whereas the association between hospitalizations and PM_2.5 proved to be negative and statistically significant. The relationship between hospital admissions and burning detected in Manaus was not significantly. PM_2.5 particulate material proved to be significantly associated with meteorological variables and the occurrence of burning. A direct link between temperature and number of fires was observed as was an inverse link between humidity and precipitation (Table 2).

The models integrating the weekly and monthly variables proved to be significant upon multiple linear regression analysis. For the weekly model, the independent variables of p < 0.05 were included (humidity, PM_2.5 and precipitation), which explained 84% of hospitalizations for respiratory disease in children living in Manaus. The monthly model showed the humidity variable as p significant which justified 86% of hospitalizations (Table 3).

DISCUSSION

Hospitalizations of children for respiratory disease in Manaus is more related to meteorological conditions, and in particular to humidity, than to exposure to smoke emanating from burning biomass and to PM_2.5 concentrations in the region.

The time series of the hospital admissions showed seasonal behavior opposite to that of the concentrations of particulate material (Figure 2a). The greatest number of hospitalizations occurred in April and the highest PM_2.5 in November.

Mean annual levels of PM_2.5 stayed around 50% above the annual standard of air quality recommended by the World Health Organization (10 µg/m³ annual mean).²⁰20. World Health Organization. Air quality guidelines: global update. Geneva; 2005. The weekly mean of the pollutant for the rainy season (13 µg/m³) proved to be 58% lower than the dry season mean (20.6 µg/m³). Compared with other regions of the Amazon, Manaus had reduced levels of PM_2.5. In Alta Floresta, northern Mato Grosso, between 1992 and 2002, concentrations of inhalable particles reached values levels higher than 100 µg/m³ between August and October, with daily highs of up to 600 µg/m³. In Rondônia, PM_2.5 levels reached 50-90 µg/m³ in the burning season.²2. Artaxo P, Gatti LV, Leal AMC, Longo KM, Lara LL, Procópio AS, et al. Química atmosférica na Amazônia: A floresta e as emissões de queimadas controlando a composição da atmosfera amazônica. Acta Amaz. 2005;35(2):185-98. DOI: http://dx.doi.org/10.1590/S0044-59672005000200008
http://dx.doi.org/10.1590/S0044-59672005... Although standards of Brazilian air quality for PM_2.5 are studied, Brazilian legislation only contains maximum values for PM_10.

Links with hospital admissions proved to be significant when grouped by week, with a greater number of environmental variables, compared to when grouped by monthly means. This indicates that similar studies evaluating environmental effects on human health are better applied over shorter time scales, such as weeks or days. Gonçalves ^ffGonçalves KS. Queimadas e atendimentos ambulatoriais por doenças respiratórias em crianças no município de Porto Velho, Rondônia [dissertação de mestrado]. Rio de Janeiro: Escola Nacional de Saúde Pública da Fiocruz; 2010. (2010) studied outpatient care in children resident in Porto Velho, organized by month, and found no significant correlation with climatic variables.

Many studies have found adverse effects referring to climatic effects and pollutants on respiratory morbidity, depending on the region studied, the sources of the emissions, the model of hospital management and number of beds available for respiratory disease, among other factors.¹1. Araújo RF, Firmino JL, Gomes Filho M, Dantas RT. Análise da relação da incidência de Infecção Respiratória Agura (IRA) com as variáveis meteorológicas em Campina Grande. Rev Fafibe. 2007;(3):1-5. , ⁴4. Bakonyi SMC, Danni-Oliveira IM, Martins LC, Braga ALF. Poluição atmosférica e doenças respiratórias em crianças na cidade de Curitiba, PR. Rev Saude Publica. 2004;38(5):695-700. DOI: http://dx.doi.org/10.1590/S0034-89102004000500012
http://dx.doi.org/10.1590/S0034-89102004...

Results of recent studies in the Brazilian Amazon have behaved in a similar was: frequency and rates of morbidity due to respiratory disease were relatively related to certain concentrations of particulate material,¹³13. Mascarenhas MDM, Vieira LC, Lanzieri TM, Leal APR, Duarte AF, Hatch DL. Poluição atmosférica devida à queima de biomassa florestal e atendimentos de emergência por doença respiratória em Rio Branco, Brasil – Setembro, 2005. J Bras Pneumol. 2008;34(1):42-6. DOI: http://dx.doi.org/10.1590/S1806-37132008000100008
http://dx.doi.org/10.1590/S1806-37132008... to periods of low air humidity and to burning in the region.⁷7. Carmo CN, Hacon SS, Longo KM, Freitas S, Ignotti E, Artaxo P, et al. Associação entre material particulado de queimadas e doenças respiratórias na região sul da Amazônia brasileira. Rev Panam Salud Publica. 2010;27(1):10-6. DOI: http://dx.doi.org/10.1590/S1020-49892010000100002
http://dx.doi.org/10.1590/S1020-49892010... , ¹⁸18. Rosa AM, Ignotti E, Hacon SS, Castro HA. Análise das internações por doenças respiratórias em Tangará da Serra – Amazônia brasileira. J Bras Pneumol. 2008;34(8):575-82. DOI: http://dx.doi.org/10.1590/S1806-37132008000800006
http://dx.doi.org/10.1590/S1806-37132008...

The time series of the hospital admissions in Manaus showed seasonal behavior clearly associated with air humidity (Figure 2a). It is possible that environmental characteristics inherent to the rainy period in the region play an important role in increasing rates of hospitalization for respiratory disease in children. In the rainy season, natural biological particle emissions predominate, originating in the intense activity of biological organisms in the forest, including: plant and insect fragments, grains of pollen, fungus, algae and fungal spores.¹¹11. Graham B, Guyon P, Artaxo P, Maenhaut W, Taylor P, Ebert M, et al. Composition and diurnal variability of the natural Amazonian aerosol. J Geophys Res Atmos. 2003;108(D24):4795. DOI: http://dx.doi.org/10.1029/2003JD004049
http://dx.doi.org/10.1029/2003JD004049... The link between these biogenic particulates and respiratory morbidity among children in Manaus is not directly proved in this study, but it deserves to be examined in specific studies evaluating their effect on children’s health.

The most frequent cause of hospitalization among children resident in Manaus during the period in question was pneumonia (in different classifications: J12, J15 and J18), flu (J10) and asthma (J45). Pneumonia is an illness of the lungs which may be caused by different microorganisms, including viruses, bacteria, parasites or fungi. Pneumonia is a condition which, if properly treated in primary care, should not end in hospitalization.¹⁷17. Rosa AM, Ignotti E, Botelho C, Castro HA, Hacon SS. Doença respiratória e sazonalidade climática em menores de 15 anos em um município da Amazônia Brasileira. J Pediatr. 2008;84(6):543-9. DOI: http://dx.doi.org/10.1590/S0021-75572008000700012
http://dx.doi.org/10.1590/S0021-75572008... The low coverage of the Family Health Program in Manaus (in 2009, 45.4% of the population) may have contributed to the increase in hospital admissions for respiratory disease.

The complexity of evaluating the effects of particles emitted from biomass burning on human health, and especially on the most vulnerable groups, is due to a series of inert-related factors of socio-economic, clinical, epidemiological and environmental importance. It is necessary to carry out wider studies, involving professionals from different areas. This knowledge is important in defining preventative public health policies, in urban and environmental planning in any municipality, as well as reinforcing the policies of continuous monitoring of air quality, benefitting the population’s quality of life and based on scientific knowledge.

Using remote sensing techniques for estimating PM_2.5 levels proved to be viable and effective, considering the lack of air quality monitoring stations in the metropolitan region of Manaus and in the majority of the Amazon region. Using remote sensing techniques is a complementary tool to surface measurements, as they are indirect, which emphasizes the importance of long-term terrestrial monitoring stations for integrated studies in the region.

ACKNOWLEDGEMENTS

Thanks to Rogério Marinho, of the Instituto Nacional de Pesquisas Espaciais, for drawing up the maps of the study; to Dennys Mourão, of the Fundação Oswaldo Cruz, for collaborating in collecting the data; to the Central Office of the Program of Instituto Nacional de Pesquisas da Amazônia , for the logistical support.

References

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